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Dissecting the regulation of pollen tube growth by modeling the interplay of hydrodynamics, cell wall and ion dynamics.

Liu J, Hussey PJ - Front Plant Sci (2014)

Bottom Line: Currently, the two main pollen tube growth models, the cell wall model and the hydrodynamic model do not appear to be reconcilable.In this way regulation of pollen tube growth by turgor is context dependent.The novel methodology developed here reveals the underlying context-dependent regulatory principle of pollen tube growth.

View Article: PubMed Central - PubMed

Affiliation: School of Biological and Biomedical Sciences, Durham University Durham, UK.

ABSTRACT
Hydrodynamics, cell wall and ion dynamics are all important properties that regulate pollen tube growth. Currently, the two main pollen tube growth models, the cell wall model and the hydrodynamic model do not appear to be reconcilable. Here we develop an integrative model for pollen tube growth and show that our model reproduces key experimental observations: (1) that the hypertonic condition leads to a much longer oscillatory period and that the hypotonic condition halves the oscillatory period; (2) that oscillations in turgor are experimentally undetectable; (3) that increasing the extracellular calcium concentration or decreasing the pH decreases the growth oscillatory amplitude; (4) that knockout of Raba4d, a member of the Rab family of small GTPase proteins, decreases pollen tube length after germination for 24 h. Using the model generated here, we reveal that (1) when cell wall extensibility is large, pollen tube may sustain growth at different volume changes and maintain relatively stable turgor; (2) turgor increases if cell wall extensibility decreases; (3) increasing turgor due to decrease in osmolarity in the media, although very small, increases volume change. However, increasing turgor due to decrease in cell wall extensibility decreases volume change. In this way regulation of pollen tube growth by turgor is context dependent. By changing the osmolarity in the media, the main regulatory points are extracellular osmolarity for water flow and turgor for the volume encompassed by the cell wall. However, if the viscosity of cell wall changes, the main regulatory points are turgor for water flow and wall extensibility for the volume encompassed by the cell wall. The novel methodology developed here reveals the underlying context-dependent regulatory principle of pollen tube growth.

No MeSH data available.


Related in: MedlinePlus

Modeling results reproduce the dependence of oscillatory periods of growth rate and pollen tube length on osmolarity in the media. Pollen tube grows in a media of 0.36 Osm. At time = 7200 s, osmolarity in the media changes to (A) 0.18 Osm; (B) 0.36 Osm (i.e., remaining unchanged); (C): 1.16 Osm following experiments (Zonia and Munnik, 2004, 2007, 2011; Zonia et al., 2006). (D): Panel (D) compares pollen tube length for the above three media conditions (top: 1.16 Osm; middle: 0.18 Osm; bottom: 0.36 Osm). In (A), the pollen tube radius linearly increases from 5 to 5.5 μm from 7200 to 9000 s. In (B), the pollen tube radius does not change (5 μm). In (C), the pollen tube radius linearly decreases from 5 to 3.5 μm from 7200 to 9000 s. In experiments, Zonia and Munnik (2004) show that, when osmolarity in the media decreases from 0.36 to 0.18 Osm, pollen tube radius increases. When osmolarity in the media increases from 0.36 to 1.16 Osm, pollen tube radius decreases.
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Figure 2: Modeling results reproduce the dependence of oscillatory periods of growth rate and pollen tube length on osmolarity in the media. Pollen tube grows in a media of 0.36 Osm. At time = 7200 s, osmolarity in the media changes to (A) 0.18 Osm; (B) 0.36 Osm (i.e., remaining unchanged); (C): 1.16 Osm following experiments (Zonia and Munnik, 2004, 2007, 2011; Zonia et al., 2006). (D): Panel (D) compares pollen tube length for the above three media conditions (top: 1.16 Osm; middle: 0.18 Osm; bottom: 0.36 Osm). In (A), the pollen tube radius linearly increases from 5 to 5.5 μm from 7200 to 9000 s. In (B), the pollen tube radius does not change (5 μm). In (C), the pollen tube radius linearly decreases from 5 to 3.5 μm from 7200 to 9000 s. In experiments, Zonia and Munnik (2004) show that, when osmolarity in the media decreases from 0.36 to 0.18 Osm, pollen tube radius increases. When osmolarity in the media increases from 0.36 to 1.16 Osm, pollen tube radius decreases.

Mentions: The model (Figure 1), which intrinsically couples hydrodynamics, cell wall and ion dynamics, reproduces the dependence of oscillatory dynamics on the osmolarity in the media. Figure 2 shows the dependence of growth rate and pollen tube length on osmolarity in the media. In isotonic media (0.36 Osm), oscillations emerge with a period of ca. 50 s. When the media becomes hypotonic (0.18 Osm), the pollen tube grows with a much shorter oscillatory period (ca. 25 s). However, when the media is hypertonic (1.16 Osm), oscillatory periods are much longer (ca. 87 s) (Zonia and Munnik, 2004, 2007, 2011; Zonia et al., 2006).


Dissecting the regulation of pollen tube growth by modeling the interplay of hydrodynamics, cell wall and ion dynamics.

Liu J, Hussey PJ - Front Plant Sci (2014)

Modeling results reproduce the dependence of oscillatory periods of growth rate and pollen tube length on osmolarity in the media. Pollen tube grows in a media of 0.36 Osm. At time = 7200 s, osmolarity in the media changes to (A) 0.18 Osm; (B) 0.36 Osm (i.e., remaining unchanged); (C): 1.16 Osm following experiments (Zonia and Munnik, 2004, 2007, 2011; Zonia et al., 2006). (D): Panel (D) compares pollen tube length for the above three media conditions (top: 1.16 Osm; middle: 0.18 Osm; bottom: 0.36 Osm). In (A), the pollen tube radius linearly increases from 5 to 5.5 μm from 7200 to 9000 s. In (B), the pollen tube radius does not change (5 μm). In (C), the pollen tube radius linearly decreases from 5 to 3.5 μm from 7200 to 9000 s. In experiments, Zonia and Munnik (2004) show that, when osmolarity in the media decreases from 0.36 to 0.18 Osm, pollen tube radius increases. When osmolarity in the media increases from 0.36 to 1.16 Osm, pollen tube radius decreases.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4127481&req=5

Figure 2: Modeling results reproduce the dependence of oscillatory periods of growth rate and pollen tube length on osmolarity in the media. Pollen tube grows in a media of 0.36 Osm. At time = 7200 s, osmolarity in the media changes to (A) 0.18 Osm; (B) 0.36 Osm (i.e., remaining unchanged); (C): 1.16 Osm following experiments (Zonia and Munnik, 2004, 2007, 2011; Zonia et al., 2006). (D): Panel (D) compares pollen tube length for the above three media conditions (top: 1.16 Osm; middle: 0.18 Osm; bottom: 0.36 Osm). In (A), the pollen tube radius linearly increases from 5 to 5.5 μm from 7200 to 9000 s. In (B), the pollen tube radius does not change (5 μm). In (C), the pollen tube radius linearly decreases from 5 to 3.5 μm from 7200 to 9000 s. In experiments, Zonia and Munnik (2004) show that, when osmolarity in the media decreases from 0.36 to 0.18 Osm, pollen tube radius increases. When osmolarity in the media increases from 0.36 to 1.16 Osm, pollen tube radius decreases.
Mentions: The model (Figure 1), which intrinsically couples hydrodynamics, cell wall and ion dynamics, reproduces the dependence of oscillatory dynamics on the osmolarity in the media. Figure 2 shows the dependence of growth rate and pollen tube length on osmolarity in the media. In isotonic media (0.36 Osm), oscillations emerge with a period of ca. 50 s. When the media becomes hypotonic (0.18 Osm), the pollen tube grows with a much shorter oscillatory period (ca. 25 s). However, when the media is hypertonic (1.16 Osm), oscillatory periods are much longer (ca. 87 s) (Zonia and Munnik, 2004, 2007, 2011; Zonia et al., 2006).

Bottom Line: Currently, the two main pollen tube growth models, the cell wall model and the hydrodynamic model do not appear to be reconcilable.In this way regulation of pollen tube growth by turgor is context dependent.The novel methodology developed here reveals the underlying context-dependent regulatory principle of pollen tube growth.

View Article: PubMed Central - PubMed

Affiliation: School of Biological and Biomedical Sciences, Durham University Durham, UK.

ABSTRACT
Hydrodynamics, cell wall and ion dynamics are all important properties that regulate pollen tube growth. Currently, the two main pollen tube growth models, the cell wall model and the hydrodynamic model do not appear to be reconcilable. Here we develop an integrative model for pollen tube growth and show that our model reproduces key experimental observations: (1) that the hypertonic condition leads to a much longer oscillatory period and that the hypotonic condition halves the oscillatory period; (2) that oscillations in turgor are experimentally undetectable; (3) that increasing the extracellular calcium concentration or decreasing the pH decreases the growth oscillatory amplitude; (4) that knockout of Raba4d, a member of the Rab family of small GTPase proteins, decreases pollen tube length after germination for 24 h. Using the model generated here, we reveal that (1) when cell wall extensibility is large, pollen tube may sustain growth at different volume changes and maintain relatively stable turgor; (2) turgor increases if cell wall extensibility decreases; (3) increasing turgor due to decrease in osmolarity in the media, although very small, increases volume change. However, increasing turgor due to decrease in cell wall extensibility decreases volume change. In this way regulation of pollen tube growth by turgor is context dependent. By changing the osmolarity in the media, the main regulatory points are extracellular osmolarity for water flow and turgor for the volume encompassed by the cell wall. However, if the viscosity of cell wall changes, the main regulatory points are turgor for water flow and wall extensibility for the volume encompassed by the cell wall. The novel methodology developed here reveals the underlying context-dependent regulatory principle of pollen tube growth.

No MeSH data available.


Related in: MedlinePlus